Functional Role Within the Feeding Circuitry

The identification of the arcuate-lateral hypothalamic pathway provides the metabolic signals from the periphery with a cortical channel and a neuroanatomical means of engaging cognitive processes in food intake behaviour. This information complements the previously dominant view that the paraventricular nucleus formed the major target for the arcuate nucleus, which focused on the neuroendocrine and autonomic response to starvation. However, the discovery of AGRP as a selective marker for arcuate nucleus NPY neurons also made it possible to map out the full extent of the projections emanating from these cells. By this approach it was demonstrated not only that the NPY and POMC neurons form almost completely parallel ascending pathways, but also that these extend well beyond the hypothalamus and include a wealth of structures, from the olfactory nuclei to the nucleus tractus solitarii.126 In this manner, the metabolic signals are in a position to directly engage numerous specialized assemblies of neurons to participate in the decision to feed or not to feed. Such a concept of distributed systems has been invoked in systems-oriented models of the regulation of feeding behaviour.127, 103,128,104 The circuitry can be compared to the basal ganglia, where incoming information has been proposed to disseminate to ensembles of "local experts"129 before converging back to a common output signal.130 In the feeding circuitry, the LHA could constitute one such "local expert", weighing in information of the arousal state or reward/hedonic qualities131 and serving as a conduit for recruiting relevant parts of the cortex; see ref 103. Other such sites include the parabrachial complex, which could add e.g. gustatory information,132 and the amygdala, which could contribute sensory cortical information pertaining to the food itself and the surrounding environment.133 Interestingly, neural information from the gastrointestinal tract via the nucleus tractus solitarii feeds into largely the same nuclei as those targeted by the arcuate nucleus, including the LHA.134-135 This relationship indicates that integration of humoral/metabolic and neural/visceral signals occurs at multiple sites, rather than collecting at a single bottleneck; see ref 103. However, the extensive reciprocal connections within this circuitry (between e.g. the LHA and the arcuate nucleus or the cerebral cortex) also suggest the existence of multiple neuronal loops, rather than a neat flow chart where information follows a straight path from sensory input into the CNS to motor output. (It should, however, be remembered that a true loop would require a signal to return to its point of origin, i.e. preferentially the very same neurons. The emerging pattern of subdivisions in the LHA may imply that this is not always the case.) Possibly, the 'feeding trace' reverberates within these loops before accumulating to a sufficient motor impetus. To summarize, while the neuroanatomy involved in integration of energy metabolism is becoming clearer, the true nature of integration within these circuits remains obscure.

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